Modern methods in peach (Современные методы в исследованиях генома персика (Prunus persica)) genome research

Peach (Prunus persica (L.) Batsch) is one of the main agricultural stone fruit crops of the family Rosaceae. Modern breeding is aimed at improving the quality of the fruit, extending the period of its production, increasing its resistance to unfavorable environmental conditions and reducing the total cost of production of cultivated varieties. However, peach breeding is an extremely long process: it takes 10–15 years from hybridization of the parental forms to obtaining fruit-bearing trees. Research into peach varieties as donors of desirable traits began in the 1980s. The first version of the peach genome was presented in 2013, and its appearance contributed to the identification and localization of loci, followed by the identification of candidate genes that control the desired trait. The development of NGS has accelerated the development of methods based on the use of diagnostic DNA markers. Approaches that allow accelerating classical breeding processes include marker-oriented selection (MOS) and genomic selection. In order to develop DNA markers associated with the traits under investigation, it is necessary to carry out preliminary mapping of loci controlling economically desirable traits and to develop linkage maps. SNP-chip approaches and genotyping by sequencing (GBS) methods are being developed. In recent years, genome-wide association analysis (GWAS) has been actively used to identify genomic loci associated with economically important traits, which requires screening of large samples of varieties for hundreds and thousands of SNPs. Study on the pangenome has shown the need to analyze a larger number of samples, since there is still not enough data to identify polymorphic regions of the genome. The aim of this review was to systematize and summarize the major advances in peach genomic research over the last 40 years: linkage and physical map construction, development of different molecular markers, full genome sequencing for peach, and existing methods for genome-wide association studies with high-density SNP markers. This review provides a theoretical basis for future GWAS analysis in order to identify high-performance markers of economically valuable traits for peach and to develop genomic selection of this crop. 

1. Abbott A.G., Georgi L., Yvergniaux D., Wang Y., Blenda A., Reighard G., Inigo M., Sosinski B. Peach: the model genome for Rosaceae. Acta Hortic. 2002;575:145­155. doi 10.17660/ActaHortic.2002.575.14

2. Abbott A.G., Arús P., Scorza R. Genetic engineering and genomics. In: Layne D., Bassi D. (Eds) The Peach Botany, Production and Uses. London: CAB International, 2008;85­105. doi 10.1079/9781845933869.0085

3. Akagi T., Hanada T., Yaegaki H., Gradziel T.M., Tao R. Genome­wide view of genetic diversity reveals paths of selection and cultivar differentiation in peach domestication. DNA Res. 2016;23(3):271­282. doi 10.1093/dnares/dsw014

4. Aranzana M.J., Abbassi E.K., Howad W., Arús P. Genetic variation, population structure and linkage disequilibrium in peach commercial varieties. BMC Genet. 2010;11:69. doi 10.1186/1471­2156­11­69

5. Arulsekar S., Parfitt D.E., Kester D.E. Comparison of isozyme vari ability in peach and almond cultivars. J Hered. 1986a;77(4):272­274. doi 10.1093/oxfordjournals.jhered.a110235

6. Arulsekar S., Parfitt D.E., Beres W., Hansche P.E. Genetics of malate dehydrogenase isozymes in the peach. J Hered. 1986b;77(1):49­51. doi 10.1093/oxfordjournals.jhered.a110166

7. Arumuganathan K., Earle E.D. Nuclear DNA content of some important plant species. Plant Mol Biol Rep.1991;9:208­218. doi 10.1007/BF02672069

8. Bailey J.S., French A.P. The Inheritance of Certain Fruit and Foliage Characters in the Peach. Amherst, MA: University of Massachusetts Press, 1949

9. Bassi D., Monet R. Botany and taxonomy. In: Layne D.R., Bassi D. (Eds) The Peach: Botany, Production and Uses. Wallingford: CAB International, 2008;1­36. doi 10.1079/9781845933869.0001

10. Batley J., Barker G., O’Sullivan H., Edwards K.J., Edwards D. Mining for single nucleotide polymorphisms and insertions/deletions in maize expressed sequence tag data. Plant Physiol. 2003;132(1): 84­91. doi 10.1104/pp.102.019422

11. Belthoff L.E., Ballard R., Abbott A., Morgens P., Callahan A., Scorza R., Baird W.V., Monet R. Development of a saturated linkage map of Prunus persica using molecular based marker systems. Acta Hortic. 1993;336:51­56. doi 10.17660/ActaHortic.1993.336.5

12. Bianco L., Cestaro A., Linsmith G., Muranty H., Denancé C., Théron A., Poncet C., … Davassi A., Laurens F., Velasco R., Durel C.E., Troggio M. Development and validation of the Axiom® Apple480K SNP genotyping array. Plant J. 2016;86(1):62­74. doi 10.1111/tpj.13145

13. Bielenberg D.G., Rauh B., Fan S., Gasic K., Abbott A.G., Reighard G.L., Okie W.R., Wells C.E. Genotyping by sequencing for SNP­based linkage map construction and QTL analysis of chilling requirement and bloom date in peach [Prunus persica (L.) Batsch]. PloS One. 2015;10(10):e0139406. doi 10.1371/journal.pone.0139406

14. Bliss F.A. Marker­assisted breeding in horticultural crops. Acta Hort. 2010;859:339­350. doi 10.17660/ActaHortic.2010.859.40

15. Byrne D.H., Sherman W.B., Bacon T.A. Stone fruit genetic pool and its exploitation for growing under warm winter conditions. In: Erez A. (Ed.) Temperate Fruit Crops in Warm Climates. Dordrecht: Springer, 2000;157­230. doi 10.1007/978­94­017­3215­4_8

16. Byrne D.H., Bassols M., Bassi D., Piagnani M., Gasic K., Reighard G., Moreno M., Pérez S. Peach. In: Badenes M.L., Byrne D.H. (Eds) Fruit Breeding. New York: Springer Science, 2012;505­570. doi 10.1007/978­1­4419­0763­9_14

17. Callahan A., Scorza R., Morgens P., Mante S., Cordts J., Cohen R. Breeding for cold hardiness: searching for genes to improve fruit quality in cold-hardy peach germplasm. HortScience. 1991;26(5):522­526. doi 10.21273/HORTSCI.26.5.522

18. Cao K., Wang L., Zhu G., Fang W., Chen C., Luo J. Genetic diversity, linkage disequilibrium, and association mapping analyses of peach (Prunus persica) landraces in China. Tree Genet Genomes. 2012; 8(5):975­990. doi 10.1007/s11295­012­0477­8

19. Cao K., Zheng Z., Wang L., Liu X., Zhu G., Fang W., Cheng S., … Li Y., Li H., Guo J., Xu X., Wang J. Comparative population genomics reveals the domestication history of the peach, Prunus persica, and human influences on perennial fruit crops. Genome Biol. 2014;15:415. doi 10.1186/s13059­014­0415­1

20. Cao K.E., Zhou Z., Wang Q., Guo J., Zhao P., Zhu G., Fang W., Chen C., Wang X., Wang X., Tian Z., Wang L. Genome­wide association study of 12 agronomic traits in peach. Nat Commun. 2016;7(1): 13246. doi 10.1038/ncomms13246

21. Cao K., Li Y., Deng C.H., Gardiner S.E., Zhu G., Fang W., Chen C., Wang X., Wang L. Comparative population genomics identified genomic regions and candidate genes associated with fruit domestication traits in peach. Plant Biotechnol J. 2019;17(10):1954­1970. doi 10.1111/pbi.13112

22. Cao K., Peng Z., Zhao X., Li Y., Liu K., Arus P., Zhu G., Deng S., Fang W., Chen C., Wang X., Wu J., Fei Z., Wang L. Pan­genome analyses of peach and its wild relatives provide insights into the genetics of disease resistance and species adaptation. BioRxiv. 2020. doi 10.1101/2020.07.13.200204

23. Cao K., Yang X., Li Y., Zhu G., Fang W., Chen C., Wang X., Wu J., Wang L. New high‐quality peach (Prunus persica L. Batsch) genome assembly to analyze the molecular evolutionary mechanism of volatile compounds in peach fruits. Plant J. 2021;108(1):281­295. doi 10.1111/tpj.15439

24. Carter G.E. Jr., Brock M.M. Identification of peach cultivars through protein analysis. HortScience. 1980;15(3):292­293 Cartwright D.A., Troggio M., Velasco R., Gutin A. Genetic mapping in the presence of genotyping errors. Genetics. 2007;176(4):2521­ 2527. doi 10.1534/genetics.106.063982

25. Chagné D., Crowhurst R.N., Troggio M., Davey M.W., Gilmore B., Lawley C., Vanderzande S., … Wilhelm L., Van de Weg E., Gardiner S.E., Bassil N., Peace C. Genome­wide SNP detection, validation, and development of an 8K SNP array for apple. PLoS One. 2012;7(2):e31745. doi 10.1371/journal.pone.0031745

26. Chaparro J.X., Durham R.E., Moore G.A., Sherman W.B. Utilization of isozyme techniques to identify peach × ‘Nonpareil’ almond hybrids. HortScience. 1987;22(2):300­302. doi 10.21273/HORTSCI.22.2.300

27. Chaparro J.X., Werner D.J., O’Malley D., Sederoff R.R. Targeted mapping and linkage analysis of morphological isozyme, and RAPD markers in peach. Theor Appl Genet. 1994;87(7):805­815. doi 10.1007/BF00221132

28. Chesnokov Yu.V., Artem’eva A.M. Association mapping in plants (review). Sel’ skokhozyaystvennaya Biologiya = Agricultural Bio logy. 2011;46(5):3­16 (in Russian)

29. Cirilli M., Baccichet I., Chiozzotto R., Silvestri C., Rossini L., Bassi D. Genetic and phenotypic analyses reveal major quantitative loci associated to fruit size and shape traits in a non­flat peach collection (P. persica L. Batsch). Hortic Res. 2021;8:232. doi 10.1038/s41438­021­00661­5

30. Collard B.C.Y., Jahufer M.Z.Z., Brouwer J.B., Pang E.C.K. An introduction to da Silva Linge C., Cai L., Fu W., Clark J., Worthington M., Rawandoozi Z., Byrne D.H., Gasic K. Multi­locus genome­wide association studies reveal fruit quality hotspots in peach genome. Front Plant Sci. 2021;12:644799. doi 10.3389/fpls.2021.644799

31. Demirel S., Pehluvan M., Aslantaş R. Evaluation of genetic diversity and population structure of peach (Prunus persica L.) genotypes using inter­simple sequence repeat (ISSR) markers. Genet Resour Crop Evol. 2024;71(3):1301­1312. doi 10.1007/s10722­023­01691­9

32. Dettori M.T., Quarta R., Verde I. A peach linkage map integrating RFLPs, SSRs, RAPDs, and morphological markers. Genome. 2001; 44(5):783­790. doi 10.1139/g01­065

33. Dirlewanger E., Moing A., Rothan C., Svanella L., Pronier V., Guye A., Plomion C., Monet R. Mapping QTLs controlling fruit quality in peach (Prunus persica (L.) Batsch). Theor Appl Genet. 1999;98: 18­31. doi 10.1007/s001220051035

34. Dirlewanger E., Cosson P., Tavaud M., Aranzana M., Poizat C., Zanetto A., Arús P., Laigret F. Development of microsatellite markers in peach [Prunus persica (L.) Batsch] and their use in genetic diversity analysis in peach and sweet cherry (Prunus avium L.). Theor Appl Genet. 2002;105(1):127­138. doi 10.1007/s00122­002­0867­7

35. Dirlewanger E., Graziano E., Joobeur T., Garriga­Calderé F., Cosson P., Howad W., Arús P. Comparative mapping and marker­assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci USA. 2004;101(23): 9891­9896. doi 10.1073/pnas.0307937101

36. Dirlewanger E., Cosson P., Boudehri K., Renaud C., Capdeville G., Tauzin Y., Laigret F., Moing A. Development of a second­generation genetic linkage map for peach [Prunus persica (L.) Batsch] and characterization of morphological traits affecting flower and fruit. Tree Genet Genomes. 2007;3:1­13. doi 10.1007/s11295­006­0053­1

37. Dirlewanger E., Claverie J., Iezzoni A.F., Wünsch A. Sweet and sour cherries: linkage maps, QTL detection and marker assisted selection. In: Folta K.M., Gardiner S.E. (Eds) Genetics and Genomics of Rosaceae. Plant Genetics and Genomics: Crops and Models. Vol. 6. New York, NY: Springer, 2009;291­313. doi 10.1007/978­0­387­77491­6_14

38. Dirlewanger E., Quero­García J., Le Dantec L., Lambert P., Ruiz D., Dondini L., Illa E., Quilot­Turion B., Audergon J.M., Tartarini S., Letourmy P., Arús P. Comparison of the genetic determinism of two key phenological traits, flowering and maturity dates, in three Prunus species: peach, apricot and sweet cherry. Heredity. 2012;109(5): 280­292. doi 10.1038/hdy.2012.38

39. Dodds P.N., Rathjen J.P. Plant immunity: towards an integrated view of plant pathogen interactions. Nat Rev Genet. 2010;11(8):539­548. doi 10.1038/nrg2812

40. Durham R.E., Moore G.A., Sherman W.B. Isozyme banding patterns and their usefulness as genetic markers in peach. J Am Soc Hortic Sci. 1987;112(6):1013­1018. doi 10.21273/JASHS.112.6.1013

41. Eduardo I., Pacheco I., Chietera G., Bassi D., Pozzi C., Vecchietti A., Rossini L. QTL analysis of fruit quality traits in two peach intraspecific populations and importance of maturity date pleiotropic effect. Tree Genet Genomes. 2011;7:323­335. doi 10.1007/s11295­010­0334­6

42. Elsadr H. A genome wide association study of flowering and fruit quality traits in peach [(Prunus persica (L.) Batsch]: Doctoral dissertation. University of Guelph, 2016

43. Elshire R.J., Glaubitz J.C., Sun Q., Poland J.A., Kawamoto K., Buckler E.S., Mitchell S.E. A robust, simple genotyping­by­sequencing (GBS) aproach for high diversity species. PloS One. 2011;6(5): e19379. doi 10.1371/journal.pone.0019379

44. Faust M., Timon B. Origin and dissemination of the peach. In: Janick J. (Ed.) Horticultural Reviews. John Wiley & Sons, Inc., 1995;331379. doi 10.1002/9780470650585.ch10

45. Font i Forcada C., Oraguzie N., Igartua E., Moreno M.Á., Gogorcena Y. Population structure and marker­trait associations for pomological traits in peach and nectarine cultivars. Tree Genet Genomes. 2013;9:331­349. doi 10.1007/s11295­012­0553­0

46. Font i Forcada C., Guajardo V., Chin­Wo S.R., Moreno M.Á. Association mapping analysis for fruit quality traits in Prunus persica using SNP markers. Front Plant Sci. 2019;9:2005. doi 10.3389/fpls.2018.02005

47. Foolad M.R., Arulsekar S., Becerra V., Bliss F.A. A genetic map of Prunus based on an interspecific cross between peach and almond. Theor Appl Genet. 1995;91:262­269. doi 10.1007/BF00220887

48. Fu W., da Silva Linge C., Gasic K. Genome­wide association study of brown rot (Monilinia spp.) tolerance in peach. Front Plant Sci. 2021;12:635914. doi 10.3389/fpls.2021.635914

49. Gao L., Gonda I., Sun H., Ma Q., Bao K., Tieman D.M., BurzynskiChang E.A., … van der Knaap E., Huang S., Klee H.J., Giovannoni J.J., Fei Z. The tomato pan­genome uncovers new genes and a rare allele regulating fruit flavor. Nat Genet. 2019;51(6):1044­1051. doi 10.1038/s41588­019­0410­2

50. Gasic K., Da Silva Linge C., Bianco L., Troggio M., Rossini L., Bassi D., Aranzana M.J., Arus P., Verde I., Peace C., Iezzoni A. Development and evaluation of a 9K SNP addition to the peach IPSC 9K SNP array v1. HortScience. 2019;54(9S):S188

51. Guajardo V., Solís S., Almada R., Saski C., Gasic K., Moreno M.Á. Genome­wide SNP identification in Prunus rootstocks germplasm collections using Genotyping­by­Sequencing: phylogenetic analysis, distribution of SNPs and prediction of their effect on gene function. Sci Rep. 2020;10(1):1467. doi 10.1038/s41598­020­58271­5

52. Guan L., Cao K., Li Y., Guo J., Xu Q., Wang L. Detection and application of genome-wide variations in peach for association and genetic relationship analysis. BMC Genet. 2019;20(1):101. doi 10.1186/s12863­019­0799­8

53. Hamblin M.T., Warburton M.L., Buckler E.S. Empirical comparison of simple sequence repeats and single nucleotide polymorphisms in assessment of maize diversity and relatedness. PLoS One. 2007;2(12): e1367. doi 10.1371/journal.pone.0001367

54. Herrero J., Cambra M., Tabuenca M.C. Cartografía de Frutales de Hueso y Pepita. Zaragoza: Estación Experimental de Aula Dei (EEAD­ CSIC), 1964

55. Hesse C.O. Peaches. In: Janick J., Moore J.N. (Eds) Advances in Fruit Breeding. West Lafayette, Ind.: Purdue University Press, 1975; 285­335

56. Hong J.H., Yi S.I., Kwon Y.S., Kim Y., Choi K.J. Genetic diversity analysis of peach [Prunus persica (L.) Batsch] varieties using SSR markers. Korean J Breed Sci. 2013;45(3):201­211. doi 10.9787/KJBS.2013.45.3.201

57. Howad W., Yamamoto T., Dirlewanger E., Testolin R., Cosson P., Cipriani G., Monforte A.J., Georgi L., Abbott A.G., Arus P. Mapping with a few plants: using selective mapping for microsatellite saturation of the Prunus reference map. Genetics. 2005;171(3):1305­1309. doi 10.1534/genetics.105.043661

58. Huang Z., Shen F., Chen Y., Cao K., Wang L. Preliminary identification of key genes controlling peach pollen fertility using genomewide association study. Plants. 2021;10(2):242. doi 10.3390/plants10020242

59. Hübner S., Bercovich N., Todesco M., Mandel J.R., Odenheimer J., Ziegler E., Lee J.S., ... Kubach T., Muños S., Langlade N.B., Burke J.M., Rieseberg L.H. Sunflower pan­genome analysis shows that hybridization altered gene content and disease resistance. Nat Plants. 2019;5(1):54­62. doi 10.1038/s41477­018­0329­0

60. International Peach Genome Initiative; Verde I., Abbott A.G., Scalab rin S., Jung S., Shu S., Marroni F., … Silva H., Salamini F., Schmutz J., Morgante M., Rokhsar D.S. The high­quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet. 2013; 45(5):487­494. doi 10.1038/ng.2586

61. Jayakodi M., Padmarasu S., Haberer G., Bonthala V.S., Gundlach H., Monat C., Lux T., ... Mayer K.F.X., Spannagl M., Li C., Mascher M., Stein N. The barley pan­genome reveals the hidden legacy of mutation breeding. Nature. 2020;588(7837):284­289. doi 10.1038/s41586­020­2947­8

62. Joiret M., Mahachie John J.M., Gusareva E.S., Van Steen K. Confounding of linkage disequilibrium patterns in large scale DNA based gene­gene interaction studies. BioData Min. 2019;12:11. doi 10.1186/s13040­019­0199­7

63. Jones N., Ougham H., Thomas H. Markers and mapping: we are all geneticists now. New Phytol. 1997;137(1):165­177. doi 10.1046/j.1469­8137.1997.00826.x

64. Joobeur T., Viruel M.A., de Vicente M.C., Jáuregui B., Ballester J., Dettori M.T., Verde I., Truco M.J., Messeguer R., Batlle I., Quarta R., Dirlewanger E., Arús P. Construction of a saturated linkage map for Prunus using an almond × peach F2 progeny. Theor Appl Genet. 1998;97:1034­1041. doi 10.1007/s001220050988

65. Jung S., Staton M., Lee T., Blenda A., Svancara R., Abbott A., Main D. GDR (Genome Database for Rosaceae): integrated web­database for Rosaceae genomics and genetics data. Nucleic Acids Res. 2008; 36:D1034­D1040. doi 10.1093/nar/gkm803

66. Jung S., Ficklin S.P., Lee T., Cheng C.­H., Blenda A., Zheng P., Yu J., Bombarely A., Cho I., Ru S., Evans K., Peace C., Abbott A.G., Mueller L.A., Olmstead M.A., Main D. The genome database for Rosaceae (GDR): year 10 update. Nucleic Acids Res. 2014;42: D1237­D1244. doi 10.1093/nar/gkt1012

67. Khlestkina E.K. Molecular markers in genetic studies and breeding. Russ J Genet Appl Res. 2014;4;236­244. https://link.springer.com/article/10.1134/S2079059714030022#citeas

68. Kim J.S., Ku Y.S., Park S.G., Kim S.H., Park H.W., Won S.Y. Anticipated polymorphic SSRs and their application based on next generation sequencing of Prunus persica. Korean J Breed Sci. 2021;53(4): 350­360. doi 10.9787/KJBS.2021.53.4.350

69. Koning­Boucoiran C.F., Esselink G.D., Vukosavljev M., van’t Westende W.P., Gitonga V.W., Krens F.A., Voorrips R.E., van de Weg W.E., Schulz D., Debener T., Maliepaard C., Arens P., Smulders M.J. Using RNA­Seq to assemble a rose transcriptome with more than 13,000 full­length expressed genes and to develop the WagRhSNP 68k Axiom SNP array for rose (Rosa L.). Front Plant Sci. 2015;6:249. doi 10.3389/fpls.2015.00249

70. Kuhn D.N., Livingstone D.S., Richards J.H., Manosalva P., Van den Berg N., Chambers A.H. Application of genomic tools to avocado (Persea americana) breeding: SNP discovery for genotyping and germplasm characterization. Sci Hortic. 2019;246:1­11. doi 10.1016/j.scienta.2018.10.011

71. Lambert P., Campoy J.A., Pacheco I., Mauroux J.B., Da Silva Linge C., Micheletti D., Bassi D., ... Pascal T., Troggio M., Aranzana M.J., Patocchi A., Arús P. Identifying SNP markers tightly associated with six major genes in peach [Prunus persica (L.) Batsch] using a highdensity SNP array with an objective of marker­assisted selection (MAS). Tree Genet Genomes. 2016;12:121. doi 10.1007/s11295­016­1080­1

72. Lander E.S., Green P., Abrahamson J., Barlow A., Daly M.J., Lincoln S.E., Newburg L. Mapmaker: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics. 1987;1(2):174­181. doi 10.1016/0888­7543(87)90010­3

73. Laucou V., Launay A., Bacilieri R., Lacombe T., Adam­Blondon A.­ F., Bérard A., Chauveau A., … Maul E., Ponnaiah M., Töpfer R., Péros J.P., Boursiquot J.M. Extended diversity analysis of cultivated grapevine Vitis vinifera with 10K genome­wide SNPs. PLoS One. 2018;13(2):e0192540. doi 10.1371/journal.pone.0192540

74. Li X., Singh J., Qin M., Li S., Zhang X., Zhang M., Khan A., Zhang S., Wu J. Development of an integrated 200K SNP genotyping array and application for genetic mapping, genome assembly improvement and genome wide association studies in pear (Pyrus). Plant Biotechnol J. 2019;17(8):1582­1594. doi 10.1111/pbi.13085

75. Li X., Wang J., Su M., Zhou J., Zhang M., Du J., Zhou H., ... Fang W., Wang L., Jia H., Gao Z., Ye Z. Single nucleotide polymorphism detection for peach gummosis disease resistance by genome­wide association study. Front Plant Sci. 2022;12:763618. doi 10.3389/fpls.2021.763618

76. Li X., Wang J., Su M., Zhang M., Hu Y., Du J., Zhou H., Yang X., Zhang X., Jia H., Gao Z., Ye Z. Multiple­statistical genome­wide association analysis and genomic prediction of fruit aroma and agronomic traits in peaches. Hortic Res. 2023;10(7):uhad117. doi 10.1093/hr/uhad117

77. Li Y.H., Zhou G., Ma J., Jiang W., Jin L.G., Zhang Z., Guo Y., ... Chang R.Z., Jiang Z., Jackson S.A., Li R., Qiu L.J. De novo assembly of soybean wild relatives for pan­genome analysis of diversity and agronomic traits. Nat Biotechnol. 2014;32(10):1045­1052. doi 10.1038/nbt.2979

78. Li Y., Cao K.E., Zhu G., Fang W., Chen C., Wang X., Zhao P., Guo J., Ding T., Guan L., Zhang Q., Guo W., Fei Z., Wang L. Genomic analy ses of an extensive collection of wild and cultivated accessions provide new insights into peach breeding history. Genome Biol. 2019;20(1):36. doi 10.1186/s13059­019­1648­9

79. Lirong W., Yong L., Gengrui Z., Weichao F., Changwen C., Ke C., Xinwei W. Peach genomics and breeding programs at Zhengzhou Fruit Research Institute, CAAS. Acta Hortic. 2020;1282:1­6. doi 10.17660/ActaHortic.2020.1282.1

80. Liu H., Cao K., Zhu G., Fang W., Chen C., Wang X., Wang L. Genomewide association analysis of red flesh character based on resequencing approach in peach. J Am Soc Hortic Sci. 2019;144(3):209­216. doi 10.21273/JASHS04622­18

81. Liu J., Bao Y., Zhong Y., Wang Q., Liu H. Genome­wide association study and transcriptome of olecranon-type traits in peach (Prunus persica L.) germplasm. BMC Genomics. 2021;22(1):702. doi 10.1186/s12864­021­08017­y

82. Liu Y., Du H., Li P., Shen Y., Peng H., Liu S., Zhou G.A., … Wang Z., Zhu B., Han B., Liang C., Tian Z. Pan­genome of wild and cultivated soybeans. Cell. 2020;182(1):162­176. doi 10.1016/j.cell.2020.05.023

83. Mardis E.R. Next­generation DNA sequencing methods. Annu Rev Genomics Hum Genet. 2008;9(1):387­402. doi 10.1146/annurev.genom.9.081307

84. Mariette S., Tavaud M., Arunyawat U., Capdeville G., Millan M., Salin F. Population structure and genetic bottleneck in sweet cherry estimated with SSRs and the gametophytic self­incompatibility locus. BMC Genet. 2010;11:77. doi 10.1186/1471­2156­11­77

85. Marrano A., Martínez­García P.J., Bianco L., Sideli G.M., Di Pierro E.A., Leslie C.A., Stevens K.A., Crepeau M.W., Troggio M., Langley C.H., Neale D.B. A new genomic tool for walnut (Juglans regia L.): development and validation of the high­density AxiomTM J. regia 700K SNP genotyping array. Plant Biotechnol J. 2019; 17(6):1027­1036. doi 10.1111/pbi.13034

86. Mas­Gómez J., Cantín C.M., Moreno M.Á., Prudencio Á.S., GómezAbajo M., Bianco L., Troggio M., Martínez­Gómez P., Rubio M., Martínez­García P.J. Exploring genome­wide diversity in the national peach (Prunus persica) germplasm collection at CITA (Zaragoza, Spain). Agronomy. 2021;11(3):481. doi 10.3390/agronomy

87. Mas­Gómez J., Cantín C.M., Moreno M.Á., Martínez­García P.J. Genetic diversity and genome-wide association study of morphological and quality traits in peach using two Spanish peach germplasm collections. Front Plant Sci. 2022;13:854770. doi 10.3389/fpls.2022.854770

88. Meng G., Zhu G., Fang W., Chen C., Wang X., Wang L., Cao K. Identification of loci for single/double flower trait by combining genomewide association analysis and bulked segregant analysis in peach (Prunus persica). Plant Breed. 2019;138(3):360­367. doi 10.1111/pbr.12673

89. Micali S., Vendramin E., Dettori M.T., Verde I. Genetics and genomics of stone fruits. In: Agricultural and Food Biotechnologies of Olea europaea and Stone Fruits. Bentham, 2015;243­307. doi 10.2174/9781608059935115010008

90. Micheletti D., Dettori M.T., Micali S., Aramini V., Pacheco I., Da Silva Linge C., Foschi S., ... Rossini L., Verde I., Laurens F., Arús P., Aranzana M.J. Whole­genome analysis of diversity and SNP­major gene association in peach germplasm. PloS One. 2015;10(9):e0136803. doi 10.1371/journal.pone.0136803

91. Monet R. Peach genetics: past present and future. Acta Hortic. 1988; 254:49­58. doi 10.17660/ActaHortic.1989.254.8

92. Monet R., Gibault B. Polymorphisme de l’alpha­amylase chez le pecher. Etude genetique. Agronomie (France). 1991;11(5):353­358 Monet R., Bastard Y., Gibault B. Genetic studies on the breeding of flat peaches. Agronomie (France). 1985;5(8):727­731

93. Monet R., Guye A., Roy M., Dachary N. Peach mendelian genetics: a short review and new results. Agronomie. 1996;16(5):321­329. doi 10.1051/agro:19960505

94. Montanari S., Bianco L., Allen B.J., Martínez­García P.J., Bassil N.V., Postman J., Knäbel M., … Langley C.H., Evans K., Dhingra A., Troggio M., Neale D.B. Development of a highly efficient Axiom™ 70 K SNP array for Pyrus and evaluation for high-density mapping and germplasm characterization. BMC Genomics. 2019;20(1):331. doi 10.1186/s12864­019­5712­3

95. Morozova O., Marra M.A. Aplications of next­generation sequencing technologies in functional genomics. Genomics. 2008;92(5):255­ 264. doi 10.1016/j.ygeno.2008.07.001

96. Nybom H., Lācis G. Recent large­scale genotyping and phenotyping of plant genetic resources of vegetatively propagated crops. Plants. 2021;10(2):415. doi 10.3390/plants10020415

97. Parfitt D.E., Arulsekar S., Ramming D.W. Identification of plum × peach hybrids by isoenzyme analysis. HortScience. 1985;20(2): 246­248

98. Paterson A.H. Making genetic maps. In: Paterson A.H. Genome Mapping in Plants. Academic Press, 1996;23­39

99. Peace C., Bassil N., Main D., Ficklin S., Rosyara U.R., Stegmeir T., Sebolt A., Gilmore B., Lawley C., Mockler T.C., Bryant D.W., Wilhelm L., Iezzoni A. Development and evaluation of a genome­wide 6K SNP array for diploid sweet cherry and tetraploid sour cherry. PLoS One. 2012;7(12):e48305. doi 10.1371/journal.pone.0048305

100. Pflieger S., Lefebvre V., Caranta C., Blattes A., Goffinet B., Palloix A. Disease resistance gene analogs as candidates for QTLs involved in pepper-pathogen interactions. Genome. 1999;42(6):1100­1110 Pozzi C., Vecchietti A. Peach structural genomics. In: Folta K.M., Gardiner S.E. (Eds) Genetics and Genomics of Rosaceae. Plant Genetics and Genomics: Crops and Models. Vol. 6. New York, NY: Springer, 2009;235­257. https://link.springer.com/book/10.1007/978­0­38777491­6

101. Purcell S., Neale B., Todd­Brown K., Thomas L., Ferreira M.A.R., Bender D., Maller J., Sklar P., de Bakker P.I.W., Daly M.J., Sham P.C. PLINK: A tool set for whole­genome association and populationbased linkage analysis. Am J Hum Genet. 2007;81(3):559­575. doi 10.1086/519795

102. Quarta R., Cedrola C., Dettori M.T., Verde I. QTL analysis of agronomic traits in a BC1 peach population. Acta Hortic. 2002;592:291­ 297. doi 10.17660/ActaHortic.2002.592.41

103. Quilot B., Wu B.H., Kervella J., Génard M., Foulongne M., Moreau K. QTL analysis of quality traits in an advanced backcross between Prunus persica cultivars and the wild relative species P. davidiana. Theor Appl Genet. 2004;109(4):884­897. doi 10.1007/s00122­0041703­z

104. Rasheed A., Hao Y., Xia X., Khan A., Xu Y., Varshney R.K., He Z. Crop breeding chips and genotyping platforms: progress, challenges, and perspectives. Mol Plant. 2017;10(8):1047­1064. doi 10.1016/j.molp.2017.06.008

105. Ru S., Main D., Evans K., Peace C. Current applications, challenges, and perspectives of marker­assisted seedling selection in Rosaceae tree fruit breeding. Tree Genet Genomes. 2015;11:8. doi 10.1007/s11295­015­0834­5

106. Salazar J.A., Ruiz D., Campoy J.A., Sánchez­Pérez R., Crisosto C.H., Martínez­García P.J., Blenda A., Jung S., Main D., MartínezGómez P., Rubio M. Quantitative trait loci (QTL) and Mendelian trait loci (MTL) analysis in Prunus: a breeding perspective and beyond. Plant Mol Biol Rep. 2013;32:1­18. doi 10.1007/s11105­013­0643­7

107. Scorza R. Gene transfer for the genetic improvement of perennial fruit and nut crops. HortScience. 1991;26(8):1033­1035

108. Scorza R., Okie W.R. Peaches (Prunus). Acta Hortic. 1991;290:177­-234. doi 10.17660/ActaHortic.1991.290.5

109. Scorza R., Mehlenbacher S.A., Lightner G.W. Inbreeding and coancestry of freestone peach cultivars of the eastern United States and implications for peach germplasm improvement. J Am Soc Hortic Sci. 1985;110(4):547­552. doi 10.21273/JASHS.110.4.547

110. Siberchicot A., Bessy A., Gueguen L., Marais G.A. Mareymap online: a user­friendly web application and database service for estimating recombination rates using physical and genetic maps. Genome Biol Evol. 2017;9(10):2506­2509. doi 10.1093/gbe/evx178

111. Smykov A., Shoferistov E., Korzin V., Mesyats N., Saplev N. Promising directions in the selection of peach, apricot and nectarine. E3S Web Conf. 2021;254:01010. doi 10.1051/e3sconf/202125401010

112. Sosinski B., Gannavarapu M., Hager L.D., Beck L.E., King G.J., Ryder C.D., Rajapakse S., Baird W.V., Ballard R.E., Abbott A.G. Characterization of microsatellite markers in peach [Prunus persica (L.) Batsch]. Theor Appl Genet. 2000;101:421­428. doi 10.1007/s001220051499

113. Tan Q., Li S., Zhang Y., Chen M., Wen B., Jiang S., Chen X., Fu X., Li D., Wu H., Wang Y., Xiao W., Li L. Chromosome­level genome assemblies of five Prunus species and genome-wide association studies for key agronomic traits in peach. Hortic Res. 2021;8(1):213. doi 10.1038/s41438­021­00648­2

114. Tanksley S.D., Young N.D., Paterson A.H., Bonierbale M.W. RFLP mapping in plant­breeding – new tools for an old science. Nat Biotechnol. 1989;7:257­264. doi 10.1038/nbt0389­257

115. Thurow L.B., Gasic K., Bassols Raseira M.C., Bonow S., Marques Castro C. Genome­wide SNP discovery through genotyping by sequencing, population structure, and linkage disequilibrium in Brazilian peach breeding germplasm. Tree Genet Genomes. 2020;16:10. doi 10.1007/s11295­019­1406­x

116. Trifonova A.A., Boris K.V., Mesyats N.V., Tsiupka V.A., Smykov A.V., Mitrofanova I.V. Genetic diversity of peach cultivars from the collection of the Nikita Botanical Garden based on SSR markers. Plants. 2021;10(12):2609. doi 10.3390/plants10122609

117. Van Ooijen J.W. Joinmap® 4. Software for the calculation of genetic linkage maps in experimental populations. ScienceOpen, Inc., 2006

118. Van Ooijen J.W. MapQTL® 6. Software for the mapping of quantitative trait loci in experimental populations of diploid species. ScienceOpen, Inc., 2009

119. Verde I., Bassil N., Scalabrin S., Gilmore B., Lawley C.T., Gasic K., Micheletti D, ... Aranzana M.J., Arús P., Iezzoni A., Morgante M., Peace C. Development and evaluation of a 9K SNP array for peach by internationally coordinated SNP detection and validation in breeding germplasm. PloS One. 2012;7(4):e35668. doi 10.1371/journal.pone.0035668

120. Verde I., Jenkins J., Dondini L., Micali S., Pagliarani G., Vend ramin E., Paris R., ... Shu S., Grimwood J., Tartarini S., Dettori M.T., Schmutz J. The Peach v2. 0 release: high­resolution linkage mapping and deep resequencing improve chromosome­scale assembly and contiguity. BMC Genomics. 2017;18(1):225. doi 10.1186/s12864­017­3606­9

121. Voorrips R.E. MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered. 2002;93(1):77­78. doi 10.1093/jhered/93.1.77

122. Wang L., Zhu G., Fang W. Peach germplasm and breeding programs at Zhengzhou in China. Acta Hortic. 2001;592:177­182. doi 10.17660/ActaHortic.2002.592.25

123. Werner D.J., Okie W.R. A history and description of the Prunus persica plant introduction collection. HortScience. 1998;33(5):787­793. doi 10.21273/HORTSCI.33.5.787

124. Winter P., Kahl G. Molecular marker technologies for plant improvement. World J Microbiol Biotechnol. 1995;11(4):438­448. doi 10.1007/BF00364619

125. Yamamoto T., Mochida K., Hayashi T. Shanhai Suimitsuto, one of the origins of Japanese peach cultivars. J Japan Soc Hortic Sci. 2003; 72(2):116­121

126. Yu J.M., Zhang Z.W., Zhu C.S., Tabanao D.A., Pressoir G., Tuinstra M.R., Kresovich S., Todhunter R.J., Buckler E.S. Simulation appraisal of the adequacy of number of background markers for relationship estimation in association mapping. Plant Genome. 2009; 2(1):63­77. doi 10.3835/plantgenome2008.09.0009

127. Yu Y., Fu J., Xu Y., Zhang J., Ren F., Zhao H., Tian S., … Wang G., Ma R., Jiang Q., Wei J., Xie H. Genome re­sequencing reveals the evolutionary history of peach fruit edibility. Nat Commun. 2018; 9(1):5404. doi 10.1038/s41467­018­07744­3

128. Zhao Q., Feng Q., Lu H., Li Y., Wang A., Tian Q., Zhan Q, ... Xu Q., Wang Z.X., Wei X., Han B., Huang X. Pan­genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat Genet. 2018;50(2):278­284. doi 10.1038/s41588­018­0041­z

129. Zurn J.D., Nyberg A., Montanari S., Postman J., Neale D., Bassil N. A new SSR fingerprinting set and its comparison to existing SSR­ and SNP­based genotyping platforms to manage Pyrus germplasm resources. Tree Genet Genomes. 2020;16:72. doi 10.1007/s11295020­01467­7